Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil

Rebelato, Marluci M.; Pontes, Gláucia M.F.; Tozetti, Alexandro M. Reproductive biology of hypoconia (Serpentes: Dipsadidae) in Brazilian subtemperate wetlands Anais da Academia Brasileira de Ciências, vol. 88, núm. 3, 2016, pp. 1699-1709 Academia Brasileira de Ciências Rio de Janeiro, Brasil

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Reproductive biology of Thamnodynastes hypoconia (Serpentes: Dipsadidae) in Brazilian subtemperate wetlands

Marluci M. Rebelato1, Gláucia M.F. Pontes2 and Alexandro M. Tozetti3

1 Instituto de Biociências, Departamento de Zoologia, Laboratório de Herpetologia, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9500, Agronomia, 91501-970 Porto Alegre, RS, Brasil 2 Setor de Herpetologia, Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCP), Avenida Ipiranga, 6681, Prédio 40, Partenon, 90619-900 Porto Alegre, RS, Brasil 3 Laboratório de Ecologia de Vertebrados Terrestres, Universidade do Vale do Rio dos Sinos, Avenida Unisinos, 950, 93022-000 São Leopoldo, RS, Brasil

Manuscript received on November 27, 2014; accepted for publication on November 27, 2015

ABSTRACT This study aimed to describe the reproductive biology of populations of Thamnodynastes hypoconia in subtemperate wetlands based on macroscopic analyses of their gonads. We analyzed 101 specimens from the southernmost regions of . The males had a greater snout-vent length, but the females reached sexual maturity with a greater body size. The reproductive cycle of the females was seasonal, with secondary vitellogenesis occurring between the winter and spring (May-October). Based on macroscopic analysis of gonads, data suggests that males have a continuous reproductive cycle. Parturition occurs between the late summer and early fall (January-April). The clutch size ranged between 4 and 16 embryos and showed no relationship with the female’s body size. The recorded reproductive frequency of T. hypoconia is low (38 %) compared to other phylogenetically related . Conversely, the studied populations appear to have a high reproductive success because it is an abundant species in the study site. Key words: ecology, Pampa, reproductive cycle, sexual maturity, .

INTRODUCTION variables, such as temperature and relative humidity, rainfall, photoperiod and lunar cycle, may affect the Reproduction is one of the primary components of reproductive cycle of snakes (Houston and Shine the life history of an organism, acting directly on 1994, Daltry et al. 1998, Sun et al. 2000). Snakes the population dynamics (Seigel and Ford 1987, can also respond to changes in their food supply Holycross and Goldberg 2001). Because they (Fitch 1982) or exhibit a pattern determined by its are ectotherms, the activities of snakes, such as phylogenetic history (Seigel and Ford 1987, Brown moving, foraging and some metabolic processes, and Shine 2006). From an evolutionary point of are directly affected by the climate (Mushinsky and view, the selective pressures in temperate regions Hébrard 1977, Nelson and Gregory 2000). Abiotic favor the establishment of seasonal reproductive

Correspondence to: Marluci Müller Rebelato cycles to synchronize the reproductive peak with E-mail: [email protected] the warmer seasons of the year (Shine 1985,

An Acad Bras Cienc (2016) 88 (3 Suppl.) 1700 Marluci M. Rebelato, Gláucia M.F. Pontes and Alexandro M. Tozetti

Duvall et al. 1982, Mathies 2011). In turn, the boreal and viviparous (Achaval and Olmos 2003). greater climatic stability and the predominance of Studies in regions with subtropical-temperate cli- higher temperatures in tropical regions appear to mates revealed a seasonal reproductive cycle in the favor the establishment of continuous reproductive females of T. hypoconia, while in the males, the cycles (Fitch 1980, Seigel and Ford 1987, Barros cycle can be continuous or seasonal (Bellini et al. et al. 2012). Evidently, not all tropical species 2013, 2014). However, due to its wide geographic have continuous reproductive cycles. In fact, in distribution, which includes northeastern, midwest- many tropical regions, there are species with ern, southeastern and southern Brazil, Paraguay, seasonal reproductive cycles (Fitch 1982, Almeida- Uruguay and Argentina (Franco 1999, Giraudo Santos and Salomão 2002, Shine 2003, Mathies 2001), it is possible that different populations show 2011) as well as continuous cycles (Saint-Girons variations in their reproductive patterns. Due to 1982). Seasonal reproductive cycles would be their relative abundance in many of the wetlands favored, even in the tropics, in situations where of southern Brazil, it is assumed that this species there is marked climate seasonality that results in possesses an efficient reproductive strategy. More- fluctuations in the availability of food resources over, being viviparous, this species is a good model (Shine 2003). to assess the reproductive patterns of Neotropical The concentration of the reproductive peak snakes, which are still rarely studied under these at certain times of the year would increase the climatic conditions. The aim of this study was to survival rate of offspring, for example, by providing describe the reproductive biology of Thamnodyn- synchrony between the births and periods with a astes hypoconia in the subtemperate, southernmost higher food supply (Marques et al. 2001, Valdujo humid environments of Brazil. et al. 2002). In addition, the relatively low winter temperatures (frequently close to 0°C) in the MATERIALS AND METHODS subtemperate regions of southern Brazil would restrict any continuous reproduction patterns in The study was developed by analyzing the Tham- the resident snake species. During the winter, the nodynastes hypoconia specimens from the Her- average temperatures of this region tend to stay petological Collections of the Universidade Fed- below the optimal temperature for embryonic eral do Rio Grande (CHFURG) and the Museu de development (Tinkle and Gibbons 1977, Shine Ciências e Tecnologia da Pontifícia Universidade 1995). Therefore, viviparous species tend to be less Católica do Rio Grande do Sul (MCP) (Appendix). affected because they can more accurately control Because there is evidence that throughout its dis- the temperature of their embryos (Seigel and Ford tribution T. hypoconia may represent a taxonomic 1987). Because of this, the study of the reproductive complex, only specimens coming from the south- cycle of viviparous snakes in colder climates ernmost Brazilian regions were selected, particu- can generate important data for understanding larly the city of Rio Grande, Rio Grande do Sul the evolutionary and adaptive processes of the (32º 02’ 06’’ S, 52º 05’ 55’’ O), where there is taxo- reproductive biology of ectotherms. nomic and climatic homogeneity. One of the numerically dominant species in To increase the sample size, additional the southernmost Brazilian wetlands is Thamno- captures were made in a preserved wetland area, dynastes hypoconia. It is a small snake belonging the Estação Ecológica do Taim (ESEC Taim), to the Tachymenini tribe (see Zaher et al. 2009, which is also located in an area in the municipality Grazziotin et al. 2012), and it is nocturnal, semi-ar- of Rio Grande (32° 50’ S and 52° 26’ O). The region

An Acad Bras Cienc (2016) 88 (3 Suppl.) Reproduction of Thamnodynastes hypoconia 1701 of origin of all of the samples is characterized for the species (Bellini et al. 2013, 2014). Ovarian by the predominance of wetlands (i.e., ponds follicles < 5 mm were considered to be in primary and permanent and temporary wetlands) that are vitellogenesis in the follicles (primary follicles). associated with a mosaic of dunes, fields and forest Embryos in early development in the follicles sandbanks (Waechter 1985). The homogeneity of were distinguished by observing their location in the landscape is primarily affected by the flood the reproductive tract, which was restricted to the cycles when the wetlands and fields become oviduct. For the males, the following information waterlogged (Gomes et al. 1987). Despite the was recorded: the length, width and thickness of regular distribution of rainfall throughout the year, the right and left testes (mm); the diameter of the the peak flood season is generally between June distal portion of the right deferent duct (mm) (see and August. The climate is classified as humid Pizzatto 2003, Almeida-Santos et al. 2006); and subtemperate, with an average annual temperature the condition of the deferent duct (coiled or not). of 18.1°C (Maluf 2000). The seasons are well The gonads were measured using a digital caliper defined and may have periods of drought in the (accuracy of 0.1 mm). The volume of the testicles spring, and the average annual rainfall is 1162 mm was used as an indicator of spermatogenic activity (Maluf 2000). (Pizzatto et al. 2008b, Gomes and Marques 2012, Collections to complement the number of Bellini et al. 2013). The testicular volume was specimens occurred between April 2012 and March estimated using the formula for the volume of an 2013 and were conducted using a visual search ellipsoid (Pleguezuelos and Feriche 1999). Despite method (Campbell and Christman 1982). The of the questionable accuracy of the testicles volume snakes were collected under permits from SISBIO measure for a real evaluation of male reproductive (no. 32620-1 and 37410-1), euthanized with the use cycle, this is a wide spread method facilitating of a barbiturate anesthetic, fixed in a solution of 10 comparisons between our and different studies % formalin and preserved in 70 % alcohol (Heyer (Pizzatto 2005, Bellini et al. 2013, 2014). et al. 1994) before assessing the reproductive state. The females were considered to be mature In the laboratory, each individual was measured when they presented with secondary follicles (≥ for their snout-vent length (SVL, in mm) using a 5 mm follicles), embryos or pleated oviducts, measuring tape (accuracy of 1 mm). To collect the indicating recent parity (Pizzatto et al. 2008a, reproductive data, the specimens were dissected Leite et al. 2009). The males were considered to via an incision in the median ventral region. For the be mature when they had turgid testes and coiled females, the following information was recorded: deferent ducts, indicating the presence of sperm the diameter of the largest ovarian follicle (mm); (Shine 1980, Almeida-Santos et al. 2014). The the largest diameter of the embryo inside the reproductive cycle of the females was characterized oviduct (mm); the number of follicles in secondary by their distribution during the year, the size of vitellogenesis (secondary follicles) or the number their ovarian follicles and the presence of embryos of embryos and the condition of oviduct (pleated in their oviducts (Shine 1977, 1988). The fecundity or extended). The determination of the follicles (litter size) was determined based on the number in secondary vitellogenesis was done posteriorly of embryos found in the oviduct, i.e., the actual using a scatterplot of the follicle measurements fertility (see Mesquita et al. 2013, Almeida-Santos (Almeida-Santos et al. 2014). The follicles ≥ 5 et al. 2014, Braz et al. 2014). The reproductive mm were considered to be secondary follicles, a frequency of the females was estimated by the value consistent with the previously recorded data percentage of reproductive females (with follicles

An Acad Bras Cienc (2016) 88 (3 Suppl.) 1702 Marluci M. Rebelato, Gláucia M.F. Pontes and Alexandro M. Tozetti

≥ 5 mm or embryos) in the sample (Pizzatto 2005). (p > 0.05) (Zar 1999). A significant result of the In the males, the volume change of the testes Rayleigh test (p < 0.05) indicates that the data are throughout the year reflected their reproductive not uniformly distributed and there is a significant cycle because the testes typically increase in size average angle or average direction (Kovach 2004), during peak spermatogenic activity (Pizzatto et al. i.e., there is seasonality in the reproductive cycles 2007a). of the studied snakes. To infer the recruitment season of the newborns To verify whether there is a relationship be- with respect to the collection dates, the SVL values tween the female size and the number of embryos of newborn and juvenile specimens received from she produces (actual fecundity), a linear correla- the collections throughout the year (see Marques et tion analysis was performed (Seigel and Ford 1987, al. 2001) were plotted on a scatterplot for a visual Shine 1992). The volume of the testes and the diam- definition of the cutoff between the newborns and eter of the deferent ducts are directly related to the young individuals/adults. Specimens with lower size of the males and their allometric relationships, SVL values were considered to be newborns or as they differ throughout the reproductive cycle young snakes. (Shine et al. 1998). Therefore, to remove the ef- To determine whether there was a significant fect of the size of the individuals on the variation in difference in the body size between the adult the diameter and volume measurements described males and females, the SVL measurements were above, we calculated the total residue of the volume compared using analysis of variance (ANOVA). To of the testes (right + left) and the diameter residue of test the existence of seasonality in the reproductive the right deferent duct relative to the SVL through- cycles of the females and males, circular statistical out the year. The residual variation in the total vol- analysis (Zar 1999) was used via the ORIANA ume of the testicles and the diameter of the right 2.02 program (Kovach 2004). The months were deferent duct between the warm months (spring/ converted to angles ranging from zero degrees summer; October-March) and the cold months (au- (January) to 330º (December) with intervals of 30. tumn/winter; April-September) was analyzed using In this analysis, each angle (month) was associated the Mann-Whitney test (U test) (Zar 1999) to indi- with the number of secondary follicles or embryos cate the reproductive cycle of the males throughout and the number of pairs of coiled deferent ducts the year (Pizzatto and Marques 2002). recorded each month. The months with the highest frequency of these records corresponded to peaks RESULTS of reproductive activity of the males and females. Of the 101 individuals that were analyzed (56 Using this method, we estimated the following: (1) specimens from collections and 45 captured during the vector average (μ), which corresponds to the this study), 63 were males (36 adults and 27 young) average period of the year in which most of the and 38 were females (31 adults and 7 young). The snakes were reproducing; (2) the circular standard average SVL of the adult males was 387.08 mm deviation (SD); and (3) the vector r, which is an (SD = 49.33; range = 270 – 480 mm) and was average concentration of the data around the circle significantly higher than that of the females (F1.64 (years), ranging from 0 (scattered data) to 1 (data = 5.48; p = 0.02), which was 361.94 mm (SD = concentrated in the same direction). The uniformity 35.75; range = 300 – 410). Although they were of the Rayleigh test (z) was used to calculate the smaller, the females reached a greater body size at probability of the null hypothesis (the data are sexual maturity (SVL = 300 mm) than the males distributed uniformly around the analyzed cycle) (SVL = 270 mm).

An Acad Bras Cienc (2016) 88 (3 Suppl.) Reproduction of Thamnodynastes hypoconia 1703

A total of 81.57 % of the females were mature follicles (< 5 mm) were found throughout the year (i.e., presence of secondary follicles, embryos and/ and secondary follicles (≥ 5 mm) were recorded or pleated oviduct). The circular statistics showed in May, August and October (winter and spring) that the reproductive cycle of the females was (Figures 1 and 2). Secondary follicles were only seasonal (p = 0.03), with embryos concentrated observed in three females (9.67 %). No specimens between October and December (spring and simultaneously presented with secondary follicles summer) (Table I; Figures 1 and 2). Primary and embryos.

Table I Results of the circular statistical analysis testing the seasonality of the reproductive cycles of the females and males of Thamnodynastes hypoconia in southernmost Brazil. Variables Reproductive females Reproductive males Number of observations (n) 11 36 Mean angle (α) 303.592° 278.479° Mean vector length (r) 0.537 0.133 Circular standard deviation (SD) 063.876° 115.162° Rayleigh test of uniformity (p) 0.03 0.53

Figure 1 - The seasonal variation in the diameter of the largest ovarian fol- licle and the largest embryo of females from Thamnodynastes hypoconia living in southernmost Brazil. Filled circles: ovarian follicle; open circles: embryo. The horizontal line indicates the size limit between the primary (< 5 mm) and secondary (≥ 5 mm) follicles.

Figure 2 - The stages of the reproductive cycles of male and female Thamnodynastes hypoconia (living in southernmost Brazil) during the different months of the year. Black bars: registered data; gray bar: inferred data.

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The actual fecundity or litter size (number of combat (Joy and Crews 1988, Crews 2000). In ad- embryos) was 7.6 ± 4.7 (range = 4 – 16) embryos dition, there was no evidence obtained in the field per female, which showed an average diameter that the males of T. hypoconia compete physically of 20.46 ± 7.48 mm (range = 12.64 to 31.8 mm). for females to mate with. An alternative explana- There was no relationship between the female SVL tion is that the larger body size of the males could value and the fecundity (R² = 0.39; p = 0.20; n = provide metabolic advantages, such as low energy 8). The reproductive frequency (the percentage of cost per unit weight. Therefore, the males tend to reproductive females in the sample) was 38 %, sug- be more vagile than females, at least during the gesting that more than half of the females that able breeding season, as has already been noted in some to reproduce were not reproducing. The smallest species of Neotropical viperids (Tozetti et al. 2009, individual analyzed had a 120 mm SVL, and those Tozetti and Martins 2013). Males that are larger that showed an SVL < 130 mm were considered than females are found in several species of Ta- to be newborns and were observed in February chymenini (Bailey 1981), excluding Thamnodyn- (summer). This cutoff point appears to be consis- astes strigatus (A. Bizerra, unpublished data) and tent because a litter of 7 newborns preserved in the Tomodon dorsatus (Bizerra et al. 2005). Nonethe- Herpetological Collection of MCP (coming from less, in Tachymenini, there are cases where there a nearby locality but outside of our study area) is no difference in size between the sexes, such as showed a mean SVL of 115 mm. Other information in Gomesophis brasiliensis (Oliveira et al. 2003), used to determine the recruitment season included Thamnodynastes chaquensis, T. hypoconia and T. an observation of two females in December (sum- strigatus (Bellini et al. 2014). mer) with embryos that were almost at parturition, Females of T. hypoconia reached sexual ma- with an average SVL of 85 mm. turity with a greater body size than the males. This A total of 42.86 % of the analyzed males were pattern has been recorded in other populations of mature (i.e., presence of turgid testes and convoluted the species in Argentina, Uruguay and Paraguay deferent ducts). There was no significant variation (Bellini et al. 2013, 2014), as well as in T. chaquen- between the volumes of the right and left testes sis and T. strigatus (Bellini et al. 2014). This pat- (U = 560; p = 0.32; N = 36). The circular statistic tern suggests that sexual maturity occurs later in suggests that the male reproductive cycle was females than in males (see Shine 1978, Vitt 1983). continuous (p = 0.53) (Table I; Figure 2). There One possible explanation for this difference is the was also no significant difference in the variation fact that the preparation for reproduction is more in the residue of the diameter of the right deferent energetically costly for females than for males duct between the hot and cold months (U = 159; p (Madsen and Shine 1994, Luiselli et al. 1996a, b). = 0.94; N = 36) nor in the variation in the residue The possibility that males have a lower metabolic of the total volume of the testicles (U = 159; p = cost associated with reproduction is enhanced by 0.94; N = 36). our data that show sexually active males through-

DISCUSSION out the year. A later maturation in females would lead to a later start of the reproductive process, giv- Our data showed that the males of Thamnodynas- ing rise to specimens with larger body sizes and fa- tes hypoconia are larger than the females, which voring larger litters (Madsen and Shine 1993, Shine is common in species where there is male com- 1993). However, we found no relationship between bat (Shine et al. 2000). However, this dimorphism the females’ size and their litter size, reinforcing the in size is not unique for species with male-male data of Bellini et al. (2013, 2014). The clutch size

An Acad Bras Cienc (2016) 88 (3 Suppl.) Reproduction of Thamnodynastes hypoconia 1705 ranged from 4 to 16 embryos per female, similar cycle. For example, in the southernmost regions of to the results of Achaval and Olmos (2003), Car- Brazil, a seasonal reproductive cycle was reported reira et al. (2005) and Bellini et al. (2013, 2014). in females from Erythrolamprus poecilogyrus (D. According to these authors, these values ​​indicate Selbach, unpublished data), whereas a continuous that T. hypoconia have a low fecundity when com- cycle was recorded in a population in the southeast pared with other snakes, including those that are (Pinto and Fernandes 2004). Therefore, it is possible phylogenetically related, such as T. dorsatus (4 to that in the southernmost regions of Brazil, the peak 26 embryos per female) (Bizzera et al. 2005). The reproductive activity occurs during the warmer lower number of embryos may be related to the months of the year, avoiding the relatively low semi-arboreal habitat of T. hypoconia (Achaval and winter temperatures. Furthermore, it is suggested Olmos 2003), due possible limitations in the use of that the seasonal cycle of reproduction favors the the vegetation by very heavy females (Pizzatto et synchrony between the birth of the newborns and al. 2007b). the period with the highest prey offering (Marques The reproductive cycle of the females was et al. 2001, Valdujo et al. 2002). seasonal, with embryos restricted to the warmer All of the examined individuals were captured months. However, the low number of available recently (less than 4 years ago), reducing the risks females in June-July (colder months), limited the of deformities in the gonads, which would interfere evaluation of the reproductive status during this with the interpretation of their cycle (Almeida- single period. However, the examined specimens Santos et al. 2014). However, we reinforce the need (including those from the collections) were cap- of histological analyzes for a real determination of tured through regular surveys using homogeneous the spermatogenesis peak (Almeida-Santos et al. sampling efforts. Therefore, the low number of 2014). specimens captured in June-July suggests a period Many studies have evaluated the reproductive when the females reduce their activity or mobility patterns of snakes in different climatic regions (Santos et al. 2012). This behavior is likely associ- (Pizzatto et al. 2008a). Generally, in temperate ated with the need to reduce energy costs and the areas, snakes have reproductive peak in the warmer accumulation of yolk in the follicles. months of the year, while in tropical areas these The parturition events occurred between peaks are distributed more irregular throughout late summer and early fall (January-April). The the year (Fitch 1982, Seigel and Ford 1987). hypothesis that mating occurs in spring and births Despite methodological limitations, our estimates in the summer has already been proposed in other indicate that the reproductive pattern of males in studies (Gudynas 1981, Carreira et al. 2005, T. hypoconia tends to be continuous. This pattern Sawaya et al. 2008). Despite the low number of was not expected due to the relatively cold climate recorded secondary follicles (N = 3), there was (subtemperate) of the Brazilian southernmost (see a trend towards an increase in the diameter over Seigel and Ford 1987). However, the seasonal the months from May to October (late fall to mid- cycle has been registered for females. Confirmation spring), corroborating the data of Bellini et al. of the male cycle, however, depends on histological (2013). However, the peak reproduction periods analyzes of their gonads. Thus, the plasticity of of T. hypoconia can differ between populations the reproductive cycle in Thamnodynastes has (Bellini et al. 2014). In addition to variations been observed in other studies evaluating different throughout the year, geographical variations appear populations (Belini et al. 2013, 2014). These data to interfere more broadly with the reproductive reinforce the idea that the phylogenetic affinities do

An Acad Bras Cienc (2016) 88 (3 Suppl.) 1706 Marluci M. Rebelato, Gláucia M.F. Pontes and Alexandro M. Tozetti not support reproductive similarities within a genus ACKNOWLEDGMENTS (Pizzatto et al. 2008a). This observation shows the The authors acknowledge the field assistance pro- importance of other elements in the definition of vided by Daniela Selbach and Paulo Ellert and the reproductive cycles, including climate complexity support provided by the employees of the Estação (Greene 1997) and food availability (Santos et al. Ecológica do Taim during the fieldwork. Addi- 2005, Seigel and Ford 1987). Thus, climatic factors tional thanks are provided to Conselho Nacional de seem to have predominant action on these cycles Desenvolvimento Científico e Tecnológico (CNPq) (Pizzatto and Marques 2002, 2006). and Coordenação de Aperfeiçoamento de Pessoal Despite the potential of males to reproduce de Nível Superior (CAPES) for their financial sup- throughout the year, the same trend was not ob- port for this study. served in the females, which suggests that there is only one breeding season per year. This hypoth- RESUMO esis is reinforced by the fact that there were no fe- O estudo teve como objetivo descrever a biologia repro- males exhibiting simultaneous secondary follicles dutiva das populações de Thamnodynastes hypoconia and embryos (Brown and Shine 2006, Pizzatto et em ambientes subtemperados úmidos baseado em aná- al. 2008b). On the converse, the low proportion of lises macroscópicas das suas gônadas. Foram analisados registered breeding females indicates that the re- 101 espécimes provenientes do extremo sul do Brasil. productive cycles are biennial or multi-year, which Os machos tiveram maior comprimento rostro-cloacal, is reinforced by the simultaneous occurrence of mas as fêmeas atingiram a maturidade sexual com maior tamanho corpóreo. O ciclo reprodutivo das fêmeas foi pregnant females and mature females without sec- sazonal, com vitelogênese secundária ocorrendo entre o ondary follicles or embryos (Bellini et al. 2013, inverno e a primavera (Maio-Outubro). Baseado na aná- 2014). Our data reveled a low proportion of repro- lise macroscópica das gônadas, os dados sugerem que ductive females of T. hypoconia in the sampling os machos tenham ciclo reprodutivo contínuo. O parto population, similar to that recorded by Bellini et ocorre entre o fim do verão e início do outono (Janeiro- al. (2013, 2014), who obtained a proportion of -Abril). O tamanho da ninhada variou entre 4 e 16 em- reproductive females of 48 %. In our study site, briões e não apresentou relação com o tamanho do corpo da fêmea. A frequência reprodutiva de T. hypoconia foi previous sampling using pitfall traps and visual baixa (38 %) quando comparada com espécies filogene- sampling (unpublished data) demonstrated that T. ticamente próximas. Por outro lado, as populações estu- hypoconia is one of the most abundant snake spe- dadas parecem ter um alto sucesso reprodutivo, uma vez cies. Being a viviparous snake should contribute que é uma espécie muito abundante no local de estudo. to their reproductive success and consequently, to Palavras-chave: ecologia, Pampa, ciclo reprodutivo, ma- their high population density in the region (Santos turidade sexual, serpentes. et al. 2012). Moreover, while it is considered to be a relatively cold climate by Neotropical standards, REFERENCES even during the winter, the daily peak temperatures Achaval F and Olmos A. 2003. Anfibios y Del often exceed 25°C, favoring thermoregulation. Uruguay. 2 ed., Graphis Impresora, Montevideo, Uruguay, 160 p. Therefore, it is possible that the reproductive suc- Almeida-Santos SM, Braz HB, Santos LC, Sueiro LR, cess is due to the continuous cycle of males and Barros VA, Rojas CA and Kasperoviczus KN. 2014. also the viviparity of the species, which would al- Biologia reprodutiva de serpentes: recomendações para a coleta e análise de dados. Herpetologia Brasileira 3: 14-24. low adjustments in the peak reproduction period of Almeida-Santos SM and Salomão MG. 2002. Reproduc- the females throughout its distribution area. tion in neotropical pitvipers, with emphasis on species of

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